Retinal ganglion cell topography and spatial resolving power in the river hippopotamus (Hippopotamus amphibius)

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The superorder Cetartiodactyla comprise an unusual mammalian cohort formed by artiodactyls (even‐toed hoofed mammals) and cetaceans (whales, dolphins, and allies) (Price, Bininda‐Emonds, & Gittleman, 2005). With ∼300 species, they occupy a wide diversity of terrestrial and aquatic environments and exhibit marked variation in foraging specialization (Foss & Prothero, 2007; Price et al., 2005). Artiodactyls are herbivores displaying adaptations for grazing and browsing, and occur in habitats with different vegetation structures ranging from open savannahs and Arctic tundras to enclosed rainforests (Foss & Prothero, 2007). In stark contrast, cetaceans are carnivores feeding mainly on crustaceans, squids, and fish and are fully adapted to aquatic environments with distinct physical properties ranging from turbid freshwater rivers to the open ocean (Wilson & Mittermeier, 2014). This diversity of trophic specializations and habitat occupation among cetartiodactyls indicates a need for substantial evolutionary plasticity of the retina to accommodate the differential roles of the visual system in their various habitats and foraging niches.
In fact, the topographic distribution of retinal ganglion cell densities shows remarkable variation between artiodactyls and cetaceans (Hughes, 1977; Mass & Supin, 2007). Artiodactyls examined to date have an elongated band of high retinal ganglion cell density (i.e., a horizontal streak) that spans the equator of the eye (Coimbra, Hart, Collin, & Manger, 2013; Hughes, 1977; Hughes & Whitteridge, 1973; Shinozaki, Hosaka, Imagawa, & Uehara, 2010). Horizontal streaks afford panoramic visual sampling of objects across the horizon and potentially facilitate the detection of predators and conspecifics (Collin, 1999; Hughes, 1977). Moreover, artiodactyls also have a concentric high‐density area within the temporal portion of the visual streak. Given its location, the temporal area enhances visual sampling in the frontal visual field which may facilitate the detection of food items (Collin, 1999; Hughes, 1977). A derived feature of the artiodactyl retina is a vertical extension of high ganglion cell density along the dorsotemporal meridian (Hughes, 1977). This dorsotemporal extension (or anakatabatic area) enhances visual sampling in the inferior visual field and may assist with feeding and control of ambulation (Hughes, 1977). The magnitude and organization of the dorsotemporal extension appear to vary as a function of the distance of the head from the ground, with short artiodactyls showing a less pronounced and flatter arrangement compared to tall artiodactyls (Coimbra et al., 2013; Hughes, 1977; Hughes & Whitteridge, 1973; Schiviz, Ruf, Kuebber‐Heiss, Schubert, & Ahnelt, 2008).
Cetaceans show a remarkably different topographic pattern of retinal ganglion cell densities compared to artiodactyls (Hughes, 1977; Mass & Supin, 2007). Although both artiodactyls and most species of cetaceans share a temporal area of high ganglion cell density, most cetaceans have an unusual concentration of ganglion cells in the nasal retina (nasal area) which is rare among terrestrial mammals (Coimbra & Manger, 2017; Coimbra et al., 2013; Hughes, 1977; Hughes & Whitteridge, 1973; Mass & Supin, 2007; Pettigrew, Bhagwandin, Haagensen, & Manger, 2010; Pettigrew & Manger, 2008; Shinozaki et al., 2010). It has been suggested that the temporal and nasal areas in cetaceans improve vision simultaneously in the frontal and posterior visual fields and therefore play a role in the detection of food items and predators (Mass & Supin, 2007). In contrast to artiodactyls, a pronounced horizontal streak is not a common feature of the retina of cetaceans, which possibly reflects their occupation of three‐dimensional aquatic environments (Mass & Supin, 2007); however, many cetacean species have a weak streak‐like band of high ganglion cell density in their ventral retina (Mass & Supin, 1995; Mass, Supin, Abramov, Mukhametov, & Rozanova, 2013; Mass & Supin, 1986).
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